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Repeated stimulus presentations commonly produce decreased neural responses-a phenomenon known as repetition suppression (RS) or adaptation-in ventral temporal cortex (VTC) of humans and nonhuman primates. However, the temporal features of RS in human VTC are not well understood. To fill this gap in knowledge, we utilized the precise spatial localization and high temporal resolution of electrocorticography (ECoG) from nine human subjects implanted with intracranial electrodes in the VTC. The subjects viewed nonrepeated and repeated images of faces with long-lagged intervals and many intervening stimuli between repeats. We report three main findings: 1) robust RS occurs in VTC for activity in high-frequency broadband (HFB), but not lower-frequency bands; 2) RS of the HFB signal is associated with lower peak magnitude (PM), lower total responses, and earlier peak responses; and 3) RS effects occur early within initial stages of stimulus processing and persist for the entire stimulus duration. We discuss these findings in the context of early and late components of visual perception, as well as theoretical models of repetition suppression.

Developmental accounts of autism spectrum disorder (ASD) state that infants and children with ASD are spontaneously less attracted by and less proficient in processing social stimuli such as faces. This is hypothesized to partly underlie social communication difficulties in ASD. While in some studies a reduced preference for social stimuli has been shown in individuals with ASD, effect sizes are moderate and vary across studies, stimuli, and designs. Eye tracking, often the methodology of choice to study social preference, conveys information about overt orienting processes but conceals covert attention, possibly resulting in an underestimation of the effects. In this study, we recorded eye tracking and electroencephalography (EEG) during fast periodic visual stimulation to address this issue. We tested 21 boys with ASD (8-12 years old) and 21 typically developing (TD) control boys, matched for age and IQ. Streams of variable images of faces were presented at 6 Hz alongside images of houses presented at 7.5 Hz or vice versa, while children were engaged in an orthogonal task. While frequency-tagged neural responses were larger in response to faces than simultaneously presented houses in both groups, this effect was much larger in TD boys than in boys with ASD. This group difference in saliency of social versus non-social processing is significant after 5 sec of stimulus presentation and holds throughout the entire trial. Although there was no interaction between group and stimulus category for simultaneously recorded eye-tracking data, eye tracking and EEG measures were strongly correlated. We conclude that frequency-tagging EEG, allowing monitoring of both overt and covert processes, provides a fast, objective and reliable measure of decreased preference for social information in ASD.

Despite being of primary importance for fundamental research and clinical studies, the relationship between local neural population activity and scalp electroencephalography (EEG) in humans remains largely unknown. Here we report simultaneous scalp and intracerebral EEG responses to face stimuli in a unique epileptic patient implanted with 27 intracerebral recording contacts in the right occipitotemporal cortex. The patient was shown images of faces appearing at a frequency of 6 Hz, which elicits neural responses at this exact frequency. Response quantification at this frequency allowed to objectively relate the neural activity measured inside and outside the brain. The patient exhibited typical 6 Hz responses on the scalp at the right occipitotemporal sites. Moreover, there was a clear spatial correspondence between these scalp responses and intracerebral signals in the right lateral inferior occipital gyrus, both in amplitude and in phase. Nevertheless, the signal measured on the scalp and inside the brain at nearby locations showed a 10-fold difference in amplitude due to electrical insulation from the head. To further quantify the relationship between the scalp and intracerebral recordings, we used an approach correlating time-varying signals at the stimulation frequency across scalp and intracerebral channels. This analysis revealed a focused and right-lateralized correspondence between the scalp and intracerebral recordings that were specific to the face stimulation is more broadly distributed in various control situations. These results demonstrate the interest of a frequency tagging approach in characterizing the electrical propagation from brain sources to scalp EEG sensors and in identifying the cortical sources of brain functions from these recordings.

Rapid individuation of conspecifics' faces is ecologically important in the human species, whether the face belongs to a familiar or unfamiliar individual. Here we tested a large group (N = 69) of epileptic patients implanted with intracerebral electrodes throughout the ventral occipito-temporal cortex (VOTC). We used a frequency-tagging visual stimulation paradigm optimized to objectively measure face individuation with direct neural recordings. This enabled providing an extensive map of the significantly larger neural responses to upright than to inverted unfamiliar faces, i.e. reflecting visual face individuation processes that go beyond physical image differences. These high-level face individuation responses are both distributed and anatomically confined to a strip of cortex running from the inferior occipital gyrus all along the lateral fusiform gyrus, with a large right hemispheric dominance. Importantly, face individuation responses are limited anteriorly to the bilateral anterior fusiform gyrus and surrounding sulci, with a near absence of significant responses in the extensively sampled temporal pole. This large-scale mapping provides original evidence that face individuation is supported by a distributed yet anatomically constrained population of neurons in the human VOTC, and highlights the importance of probing this function with face stimuli devoid of associated semantic, verbal and affective information.

Individuals with autism spectrum disorder (ASD) have difficulties with social communication and interaction. The social motivation hypothesis states that a reduced interest in social stimuli may partly underlie these difficulties. Thus far, however, it has been challenging to quantify individual differences in social orientation and interest, and to pinpoint the neural underpinnings of it. In this study, we tested the neural sensitivity for social versus non-social information in 21 boys with ASD (8-12 years old) and 21 typically developing (TD) control boys, matched for age and IQ, while children were engaged in an orthogonal task. We recorded electroencephalography (EEG) during fast periodic visual stimulation (FPVS) of social versus non-social stimuli to obtain an objective implicit neural measure of relative social bias. Streams of variable images of faces and houses were superimposed, and each stream of stimuli was tagged with a particular presentation rate (i.e., 6 and 7.5 Hz or ). This frequency-tagging method allows disentangling the respective neural responses evoked by the different streams of stimuli. Moreover, by using superimposed stimuli, we controlled for possible effects of preferential looking, spatial attention, and disengagement. Based on four trials of 60 s, we observed a significant three-way interaction. In the control group, the frequency-tagged neural responses to faces were larger than those to houses, especially in lateral occipito-temporal channels, while the responses to houses were larger over medial occipital channels. In the ASD group, however, faces and houses did not elicit significantly different neural responses in any of the regions. Given the short recording time of the frequency-tagging paradigm with multiple simultaneous inputs and the robustness of the individual responses, the method could be used as a sensitive marker of social preference in a wide range of populations, including younger and challenging populations.

The extent to which faces and written words share neural circuitry in the human brain is actively debated. We provide an original contribution to this debate by comparing face-selective and word-selective responses in a large group of patients (N=37) implanted with intracerebral electrodes in the ventral occipito-temporal cortex (VOTC). Both face-selective (i.e., significantly different responses to faces vs. nonface objects) and word-selective (i.e., significantly different responses to words vs. pseudofonts) neural activity is isolated through frequency-tagging (Jonas et al., 2016; Lochy et al., 2018, respectively). Critically, this approach allows disentangling category-selective neural responses from general visual responses. Overall, we find that 69.26% of significant contacts show either face- or word-selectivity, with the expected right and left hemispheric dominance, respectively (Fig.1A,B). Moreover, the center of mass for word-contacts is more lateral than for face-contacts, with no differences in postero-anterior axis (Fig.2A). Spatial dissociations are also found within core regions of face and word processing, with a medio-lateral dissociation in the fusiform gyrus (FG) and surrounding sulci (FG+sulci;Fig.2B), while a postero-anterior dissociation is found in the inferior occipital gyrus (IOG;Fig.2C). Despite their spatial dissociations in the FG+sulci and IOG, most overlap in category-selective responses is found in these regions (Fig.1C). Critically, in the overlap-contacts, across the whole brain or specifically in the FG+sulci, between-category (word-face) selective-amplitudes showed no-to-weak correlations, despite strong correlations for within-category (face-face, word-word) selective-amplitudes (Fig.3A), and a strong correlation in non-selective general-amplitudes to words-faces. Moreover, substantial overlap and no-to-weak correlations were observed between faces and a control category (houses) known to be functionally dissociated from faces. O